208 VOL. 49(3) 2019: 208 - 212

http://dx.doi.org/10.1590/1809-4392201901061

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ACTAAMAZONICA

CITE AS: Fraga, R. de; Torralvo, K. 2019. New record of the fringed leaf frog, Cruziohyla craspedopus (Anura: Phyllomedusidae) extends its eastern range limit. Acta Amazonica 49: 208-212.

New record of the fringed leaf frog, Cruziohyla craspedopus (Anura: Phyllomedusidae) extends its eastern range limitRafael de FRAGA1* , Kelly TORRALVO2

1 Universidade Federal do Oeste do Pará – UFOPA, Programa de Pós-Graduação em Recursos Naturais Amazônicos, Av. Mendonça Furtado, 2240, Aldeia, 68040-050, Santarém, Pará, Brasil

2 Instituto Nacional de Pesquisas da Amazônia – INPA, Programa de Pós-Graduação em Ecologia, Av. Efigênio Sales, 2239, Aleixo, 69060-020, Manaus, Amazonas, Brasil* Corresponding author: r.defraga@gmail.com; https://orcid.org/0000-0002-9900-4276

ABSTRACT The fringed leaf frog, Cruziohyla craspedopus is rarely sampled in the Brazilian Amazon, probably due to low detection probability associated with its arboreal habit. The knowledge about the species’ distribution stems from successive additions of occasional occurrence records, which indicate that the species is widely distributed throughout Amazonia. We present new occurrence records to update the geographic range of the species, which is hereby extended 224 km to the northeast. We also present morphological data from collected specimens and discuss the updated range from the geographic and ecological points of view. We show that the range of the leaf frog crosses several main tributaries along the southern bank of the Amazonas River, although the species occurrence is apparently limited by a minimum tree cover of 70%.

KEYWORDS: Amazon Basin, detectability, Tapajós, tree cover

Novo registro de ocorrência da perereca-franjada, Cruziohyla craspedopus (Anura: Phyllomedusidae) estende o limite oriental de sua distribuição RESUMOA perereca franjada, Cruziohyla craspedopus é raramente amostrada na Amazônia brasileira, provavelmente devido à baixa probabilidade de detecção associada ao seu hábito arborícola. A distribuição geográfica conhecida da espécie é resultado da adição sucessiva de registros ocasionais de ocorrência, que indicam que ela é amplamente distribuída na Amazônia. Nós apresentamos novos pontos de ocorrência para atualizar a distribuição geográfica da espécie, estendendo-a em 224 km na direção nordeste. Nós também apresentamos dados morfológicos dos espécimes coletados e discutimos a distribuição atualizada sob pontos de vista geográfico e ecológico. Mostramos que a distribuição de pererecas franjadas cruza vários tributários da margem sul do Rio Amazonas, embora esteja aparentemente limitada por cobertura arbórea mínima de 70%.

PALAVRAS-CHAVE: Bacia Amazônica, cobertura arbórea, detectabilidade, Tapajós

The genus Cruziohyla Faivovich, Haddad, Garcia, Frost, Campbell, and Wheeler 2005 comprises three species of moderate to large sized treefrogs, closely related to Agalychnis Cope, 1864 (Gray 2018). Among the Cruziohyla species, an impressive combination of colors, blotches, stripes and fringes makes the fringed leaf frog Cruziohyla craspedopus (Funkhouser 1957) easily distinguishable from C. calcarifer (Boulenger, 1902) and C. sylviae Gray, 2018. The species inhabits dense lowland-rainforests in Ecuador, Colombia, Peru and Brazil (Frost 2019), and photographic records (although not in formal voucher-based publications) exist for Bolivia (see <http://sernap.gob.bo/blog/la-rana-de-los-

arboles-habita-en-el-madidi/> and <https://www.facebook.com/groups/172267329493705/>).

Cruziohyla craspedopus has rarely been found in anuran surveys, probably due to its arboreal habits, as sampling frogs in high plant strata depends on climbing or surveying trees from suspended platforms (Lynch 2005). Despite lack of statistical support, it has been suggested that finding C. craspedopus is restricted to unpredictable breeding events, when individuals migrate vertically to low strata of the understory (Hoogmoed and Cadle 1991; Block et al. 2003; Moraes and Pavan 2017). The geographical range of the species has thus been determined through the publication of

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occasional occurrence data (Rodríguez and Duellman 1994; Lima et al. 2003; Meneghelli et al. 2011; Rodrigues et al. 2011; Venancio et al. 2014; Bitar et al. 2015; Núñez et al. 2015; Moraes and Pavan 2017), which indicate that C. craspedopus is widely distributed across Amazonia (Moraes and Pavan 2017), as had been predicted by Hoogmoed and Cadle (1991).

Here we report new distribution records of C. craspedopus that extend its easternmost distribution limit on the east bank of the Tapajós River (eastern Brazilian Amazon). Additionally, we present morphological data and discuss the distribution of C. craspedopus in relation to the main rivers of the Amazon Basin and a landsat-based tree cover distribution (Sexton et al. 2013). Tree cover is thought to be an important factor affecting species distribution and connectivity, as it determines availability of foraging, resting and reproductive sites. We used the raster R-package (Hijmans 2019) to extract data on the percentage of tree cover from each geographic coordinate.

On February 6–12 2019 we found three adult females of C. craspedopus in the Tapajós National Forest (3º21’21.0’’S, 54º57’01.7’’W, 204 m asl), a federal reserve covering about 527,000 ha of rainforest in the eastern Brazilian Amazon (municipality of Belterra, Pará state). The specimens were found close together (2–22 m apart), perched at about 2.5 m above ground in a non-floodable forest (25.9 ºC, 93% relative humidity). The perches were thin tree branches, located on the edge of a small unpaved road. Several puddles on the road were constantly used as calling and spawning sites by other frog species [e.g. Leptodactylus paraenesis Heyer, 2005; Rhinella major (Müller and Hellmich, 1936); Rhinella marina (Linnaeus, 1758); Pithecopus hypochondrialis (Daudin, 1800)], but we observed no reproductive activity of C. craspedopus. However, we found gravid females with mature oocytes, which suggests that individuals were reproductively active.

The species was identified by a combination of dark-green dorsal surface with gray-blueish irregular blotches (Figure 1a), bright-orange ventral surface (Figure 1b), vertical dark bars on a yellow background in the flanks, thighs and forearms, narrow dermal fringes on the lower jaw and on the outer edge of the forearm, and well-developed fringes on the outer edge of the tarsus (Funkhouser 1957; Hoogmoed and Cadle 1991; Gray 2018). Specimens were collected under IBAMA/SISBIO license nr. 67545-1/2019, and deposited in the herpetological collection of Universidade Federal do Oeste do Pará (UFOPA), Santarém, Pará, Brazil. Additional morphological data (based on Moraes and Pavan 2017) and voucher numbers of the specimens are provided in Table 1.

This is the first record of C. craspedopus east of the Tapajós River, which extends the species’ range 224 km northeast from its previously known easternmost locality (Parque Nacional da Amazônia, Pará, Brazil; Moraes and Pavan 2017). The updated map (Figure 2) and locality record list (Table 2) show that the species is widely distributed throughout the Amazonian lowland-

forests, crossing several of the main southern tributaries of the Amazonas River. To the north, the species is apparently limited by the Japurá River, and has not been reported north of the Amazonas River from the border between Brazil and Colombia. Biogeographic studies should focus on testing the hypothesis that the strength of the Amazonas River as a barrier to the species dispersal increases downstream. To the east, the species reaches the interfluve between the Tapajós and Iriri rivers, and possibly extends to the west bank of the Xingu River. To the west, the species is limited by the Andes, and its southernmost record lies in the Andean piedmont of Madidi National Park, Bolivia

Table 1. Morphological data (mm) of three Cruziohyla craspedopus specimens from the Tapajós National Forest, Pará, Brazil (identified by their collection voucher numbers). SVL: snout-vent length, FAL: forearm length from distal edge of hand to outer edge of flexed elbow, HA: hand length from distal edge of hand to tip of finger III, TL: tibia length from proximal edge of flexed knee to heel, FL: foot length from proximal edge of inner metatarsal tubercle to tip of Toe IV, HW: head width at level of angle of jaw, HL: head length from angle of jaw to tip of snout, ED: eye diameter, IN: internarial distance, IO: interorbital distance, EN: eye–nostril distance, TD: tympanum diameter, WFD: finger III disc width, WTD: toe IV disc width, and THL: thigh length.

Parameter UFOPA-H 1486 UFOPA-H 1487 UFOPA-H 1488

Sex Female Female Female

SVL 76.19 73.79 74.84

FAL 15.82 14.48 14.46

HA 25.69 24.72 25.36

TL 41.96 41.65 40.30

FL 30.04 28.64 29.86

HW 25.15 23.55 25.12

HL 22.15 22.97 22.79

ED 4.84 5.48 5.56

IN 6.80 7.12 6.68

IO 19.11 19.06 19.23

EN 9.23 8.53 7.32

TD 4.63 4.31 5.16

WFD 5.85 5.60 5.62

WTD 4.86 5.12 4.58

THL 38.13 36.15 36.65

Figure 1. Dorsal (A) and ventral (B) views of Cruziohyla craspedopus from the Tapajós National Forest, eastern Brazilian Amazon. Female, 76.19 mm SVL, UFOPA-H 1486. This figure is in color in the electronic version.

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Table 2. Occurrence records of Cruziohyla craspedopus in Amazonia (plotted in Figure 2). The type locality is in bold; NV = photographic records in informal non-voucher-based electronic sources; # = coordinates are estimates for imprecise locality reports by the author(s) of the record.

Locality Longitude Latitude ReferenceKunsunts-Shuar Center, Zamora-Chinchipe, Ecuador -78.639200 -4.316639 Read and Ron (2018)Morona-Santiago, Santiago River, Ecuador -78.072034 -3.110383 Hoogmoed and Cadle (1991)Jatún Biological Station, Pastaza, Ecuador -77.616000 -1.066600 Read and Ron (2018)Villano, Pastaza, Ecuador -77.534790 -1.476040 Read and Ron (2018)Ishpingo River, Pastaza, Ecuador -76.858330 -2.538666 Read and Ron (2018)Bobonaza River, Chicherota, Pastaza, Ecuador -76.633000 -2.366600 Funkhouser (1957)Limoncocha, Orellana, Pastaza, Ecuador -76.625972 -0.507551 Hoogmoed and Cadle (1991)Shiona, Pastaza, Ecuador -76.459999 -2.010000 Read and Ron (2018)Yasuní National Park, Orellana, Ecuador -76.401167 -0.677166 Read and Ron (2018)Cueva Boyopare, Orellana, Ecuador -76.399511 -0.809494 Read and Ron (2018)Napo River, Sucumbíos, Ecuador -76.364930 -0.508680 Read and Ron (2018)Cuyabeno Reserve, Sucumbíos, Ecuador -76.181660 -0.009700 Read and Ron (2018)Tiputini Biodiversity Station, Sucumbíos, Ecuador -76.171944 -0.618056 Read and Ron (2018)Comunidad Samona, Orelanna, Ecuador -75.967590 -0.571890 Read and Ron (2018)Yasuní National Park, Orellana, Ecuador -75.964000 -0.934000 Read and Ron (2018)Iquitos Region, Peru -73.487502 -3.684978 Rodríguez and Duellman (1993)Tarauacá, Acre, Brazil -71.451600 -7.978100 Venancio et al. (2014)Cocha Cashu Biological Station, Madre de Dios, Peru -71.336928 -11.970719 Hoogmoed and Cadle (1991)Leticia, Amazonas, Colombia # -69.960314 -3.950472 Ruiz-Carranza et al. (1993)Tambopata Reserve, Madre de Dios, Peru -69.275150 -12.965263 Hoogmoed and Cadle (1991)Madidi National Park, La Paz, Bolivia # -68.350051 -14.200972 NV*El Sena, Pando, Bolivia # -67.252281 -11.555366 NV**Cuniã Ecological Station, Rondônia, Brazil -63.483300 -8.106500 Meneghelli et al. (2011)Castanho, Amazonas, Brazil -59.860500 -3.354600 Lima et al. (2003)São Nicolau Farm, Cotriguaçu, Mato Grosso, Brazil -58.249300 -9.854600 Rodrigues et al. (2011)Jacareacanga, Pará, Brazil -57.683100 -6.088500 Bitar et al. (2015)Amazonas National Park, Pará, Brazil -56.441400 -4.707700 Moraes and Pavan (2017)Tapajós National Forest, Pará, Brazil -54.950472 -3.357500 this studyTapajós National Forest, Pará, Brazil -54.950308 -3.357389 this studyTapajós National Forest, Pará, Brazil -54.950306 -3.357389 this study

* <http://sernap.gob.bo/blog/la-rana-de-los-arboles-habita-en-el-madidi/>; ** <https://www.facebook.com/groups/172267329493705/>)

Figure 2. Updated distribution of Cruziohyla craspedopus in Amazonia. The star is the type-locality, circles are literature data, squares are photographic records reported in newsfeeds with no voucher specimens, and the triangle represents the specimens reported in this study. Locality details are in Table 2. This figure is in color in the electronic version.

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(Table 2, Figure 2). In Brazil, species is limited to the south by the contact zone between dense forests and Cerrado savannas and the agricultural frontier known as the arc of deforestation (Fearnside 2005). Although C. craspedopus has been classified as “Least Concern” by IUCN (Angulo et al. 2004), the southern region of its range, where accelerated habitat loss is occurring, should be prioritized for updating its conservation assessment.

Data from the landsat-based tree cover distribution showed that records of C. craspedopus are limited to localities with a minimum tree cover of 70% along a relatively wide altitudinal gradient (30–1600 m asl). This may be related to biological traits of the species, as the use of high plant strata during non-reproductive periods (Moraes and Pavan 2017), and the reproductive dependence on the availability of water accumulated in natural (Turell et al. 2016) or artificial (Wizen 2017) reservoirs. The fact that other species with a similar requirement [e.g. Osteocephalus aff. oophagus, Trachycephalus resinifictrix (Goeldi, 1907); Lima et al. 2012] were commonly sampled visually and acoustically during our field work suggests that the lack of reproductive sites is not a limiting factor for the occurrence of C. craspedopus. Additionally, tadpoles and metamorphs were observed in poor-quality human-made water reservoirs, suggesting that water quality does not limit the reproduction of the species (Wizen 2017). However, even reproductive sites with poor water quality were surrounded by trees, which suggests tree cover as a major factor affecting the species’ occurrence. Distribution modeling of C. craspedopus should focus on quantitative variables of vegetation structure, to explicitly test the effects of reproductive vertical migration from the canopy to the understory on detection probabilities (Hoogmoed and Cadle 1991; Block et al. 2003; Moraes and Pavan 2017), and the hypothesis that height and density of vegetation are positively correlated with frog densities.

ACKNOWLEDGMENTS We thank Edivaldo Farias, Jony Oliveira and the COOMFLONA for field assistance. Logistics was supported by Instituto Nacional de Pesquisas da Amazônia (INPA), Centro de Estudos Integrados da Biodiversidade Amazônica (CENBAM), Programa de Pesquisas em Biodiversidade (PPBio), Universidade Federal do Oeste do Pará (UFOPA), Fundação de Amparo à Pesquisas do Estado do Amazonas (FAPEAM), and Instituto Chico Mendes para Conservação da Biodiversidade (ICMBio). Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and FAPEAM provided scholarships to RDF and KT, respectively.

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RECEIVED: 15/03/2019ACCEPTED: 22/05/2019ASSOCIATE EDITOR: Claudia Keller